European Journal of Neuroscience
European Journal of Neuroscience, pp. 1–6, 2014
doi:10.1111/ejn.12492
Transcranial direct current stimulation reduces the cost of
performing a cognitive task on gait and postural control
Junhong Zhou,1 Ying Hao,1,2 Ye Wang,1 Azizah Jor’dan,2,3 Alvaro Pascual-Leone,3,4 Jue Zhang,1,5 Jing Fang1,5
and Brad Manor2,3,6
1
Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA, USA
3
Harvard Medical School, Boston, MA, USA
4
Department of Neurology, Berenson–Allen Center for Noninvasive Brain Stimulation, Beth Israel Deaconess Medical Center,
Boston, MA, USA
5
College of Engineering, Peking University, Beijing, China
6
Institute for Aging Research, Hebrew SeniorLife, Roslindale, MA, USA
2
Keywords: balance, dual task, human, noninvasive, standing, walking
Abstract
This proof-of-concept, double-blind study was designed to determine the effects of transcranial direct current stimulation (tDCS)
on the ‘cost’ of performing a secondary cognitive task on gait and postural control in healthy young adults. Twenty adults aged
22 2 years completed two separate double-blind visits in which gait and postural control were assessed immediately before
and after a 20 min session of either real or sham tDCS (1.5 mA) targeting the left dorsolateral prefrontal cortex. Gait speed and
stride duration variability, along with standing postural sway speed and area, were recorded under normal conditions and while
simultaneously performing a serial-subtraction cognitive task. The dual task cost was calculated as the percent change in each
outcome from normal to dual task conditions. tDCS was well tolerated by all subjects. Stimulation did not alter gait or postural
control under normal conditions. As compared with sham stimulation, real tDCS led to increased gait speed (P = 0.006), as well
as decreased standing postural sway speed (P = 0.01) and area (P = 0.01), when performing the serial-subtraction task. Real
tDCS also diminished (P < 0.01) the dual task cost on each of these outcomes. No effects of tDCS were observed for stride duration variability. A single session of tDCS targeting the left dorsolateral prefrontal cortex improved the ability to adapt gait and postural control to a concurrent cognitive task and reduced the cost normally associated with such dual tasking. These results
highlight the involvement of cortical brain networks in gait and postural control, and implicate the modulation of prefrontal cortical
excitability as a potential therapeutic intervention.
Introduction
The control of standing and walking is not autonomous as once
believed, but instead depends upon a host of cognitive functions and
underlying brain networks (Yogev-Seligmann et al., 2008). Moreover, these essential human behaviors are most often performed in
unison with concurrent cognitive tasks (Huxhold et al., 2006). Considerable research indicates that, as compared with normal conditions, cognitive ‘dual tasking’ alters both gait (Dubost et al., 2006)
and postural control (Prado et al., 2007). This ‘cost’ of performing
a cognitive task [which is often greater in aging (Lindenberger
et al., 2000; Rankin et al., 2000) and disease (Teasdale et al., 1993;
Marsh & Geel, 2000; Yardley et al., 2001; Hausdorff et al., 2008)]
suggests that these tasks interfere with one another as they call upon
shared networks within the brain (Montero-Odasso et al., 2012a).
Correspondence: Jue Zhang, 1Academy for Advanced Interdisciplinary Studies, as
above.
E-mail: [email protected]
Received 26 September 2013, revised 4 December 2013, accepted 22 December 2013
As such, strategies aimed at modulating neural activity within these
networks may optimise the ability to dual task and maximise functional capacity within numerous populations.
Transcranial direct current stimulation (tDCS) is one noninvasive
and safe strategy to modulate neural activity by sending low-amplitude currents between two or more surface electrodes placed upon
the scalp. Approximately 20 min of tDCS alters cortical excitability
for up to 40 min (Ragert et al., 2008). Although the mechanisms
are not entirely clear, tDCS targeting the left dorsolateral prefrontal
cortex (dlPFC) acutely improves a host of cognitive and motor
functions during this period, including problem solving (Metuki
et al., 2012), decision making (Hecht et al., 2010), working memory (Fregni et al., 2005; Javadi & Walsh, 2011a; Javadi et al.,
2011b), selective attention (Gladwin et al., 2012) and movement
accuracy during reaching tasks (Reis & Fritsch, 2011), in healthy
younger and/or older adults. However, it is unknown if tDCSinduced modulation of neural activity within this region can
enhance the ability to stand and walk while simultaneously performing a cognitive task.
© 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
2 J. Zhou et al.
The goal of this study was to determine the acute effects of facilitating neural activity within the left dlPFC on gait and postural control when walking and standing under normal and cognitive dual
task conditions in healthy young adults. We hypothesised that, as
compared with sham (i.e. control) tDCS, a single 20 min session of
real tDCS would reduce the cost of performing a cognitive dual task
on markers of gait and postural control. We tested this hypothesis
by conducting a double-blind proof-of-concept study in a cohort of
healthy young adults.
Materials and methods
Subjects
Twenty healthy young adults (10 men and 10 women, age
22 2 years, height 1.7 0.1 m, body mass 65 10 kg) were
recruited and provided written informed consent conforming with
The Code of Ethics of the World Medical Association (Declaration
of Helsinki) as approved by the Institutional Review Board of
Peking University First Hospital, Beijing. All subjects were righthanded as determined by the Edinburgh Handedness Inventory
(Oldfield, 1971). Exclusion criteria included any acute medical condition requiring hospitalisation within the past 6 months, the use of
centrally-acting medication, as well as any self-reported cardiovascular disease, neurological disease, musculoskeletal disorder, or any
other condition that may influence physical function.
Experimental protocol
All testing was performed at the Sport Science Research Center,
Beijing Sport University. Subjects completed two separate study visits at the same time of day separated by 1 week (Fig. 1). On each
visit, gait and postural control were assessed immediately before
and after either real or sham tDCS, as described in the following
sections. The real and sham tDCS conditions were randomised and
double-blinded, i.e. subjects and testers were not aware of the tDCS
condition, and stimulation was administered by a research assistant
uninvolved in any other assessment procedure. At the end of
each study visit, subjects completed a short questionnaire (Brunoni
et al., 2011) surveying for potential adverse effects associated with
tDCS.
Transcranial direct current stimulation procedures
Noninvasive tDCS was delivered by study personnel uninvolved
with any other study procedure. We used a battery-driven electrical stimulator (Chattanooga Iontoâ Iontophoresis System) connected to a pair of saline-soaked 35 cm2 synthetic surface sponge
electrodes placed on the scalp. The anode was placed over the left
dlPFC (i.e. the F3 region of the 10/20 electroencephalographic
electrode placement system) and the cathode over the right supraorbital region (Boggio et al., 2008). This montage is thought to
induce a facilitation of activity within the left prefrontal cortex
(under the anode) (Fecteau et al., 2007; Javadi et al., 2011) and
has been shown to acutely enhance numerous cognitive functions.
The real tDCS condition consisted of 20 min of continuous stimulation at a target intensity of 1.5 mA. This amount of stimulation
is safe for healthy young adults (Herwig et al., 2003) and has
been shown to induce acute changes in cortical excitability
(Nitsche & Paulus, 2000) and numerous cognitive functions
(Gandiga et al., 2006). At the beginning of each session, stimulation was increased manually from 0.1 to 1.5 mA in 0.1 mA increments. Subjects were instructed to notify study personnel if the
stimulation became uncomfortable. In this instance, stimulation
intensity was set to 0.1 mA below the highest intensity level
reached. Current was automatically ramped down at the end of the
session. For the sham condition, we followed an inactive stimulation protocol, as compared with an ‘off-target’ active protocol, in
order to minimise participant risk (Davis et al., 2013). On this
day, the same electrode montage and session duration were used;
however, the current was automatically ramped down at 60 s after
the current was manually increased to target level by the technician. This is a reliable control as sensations arising from tDCS
diminish considerably after the first minute of stimulation (Gandiga
et al., 2006).
Assessments of gait and postural control
Within each of the four assessment periods (i.e. before and after real
and sham tDCS), the testing order of each domain (i.e. gait and postural control) was randomised. Within each domain, multiple trials
were completed, also in random order, under different experimental
conditions as described below.
Gait was assessed along a custom-built 50 m indoor walkway
instrumented with force sensors (resolution 4 sensors/cm2, sampling
frequency 100 Hz) to record foot pressure patterns. Two trials were
completed under each of two different conditions: walking normally
and walking while performing a cognitive task. The cognitive task
consisted of verbalised, serial subtractions of three from a random
three-digit number between 400 and 500. Subjects were instructed
to walk at their preferred speed before each trial. No instructions
were given regarding task prioritisation within dual task trials. In
addition to stance phase plantar pressure distributions, the time taken
to complete each trial and cognitive task responses were manually
recorded and saved for offline analysis.
Postural control was assessed by measuring postural sway as subjects stood on a stationary force platform (Kistler Instrument Corp.,
Amherst, NY, USA). Two 60 s trials were completed under three
different experimental conditions: standing with eyes open, eyes
closed, and eyes open with cognitive dual task, i.e. simultaneous
performance of the same serial-subtraction task as described in the
previous paragraph. Subjects were instructed to stand as still as possible prior to each trial. During each trial, postural control was measured by recording center-of-pressure (COP) fluctuations at a
sampling frequency of 1000 Hz. Cognitive responses were also
manually recorded during dual task trials.
Fig. 1. Study protocol. Subjects completed two study visits separated by 1 week. Each visit was completed at the same time of day. During each visit, gait
and postural control were assessed immediately before and after either real or sham tDCS targeting the left dlPFC. The order of tDCS condition was
randomised, as was the testing order of gait and postural control within each assessment period.
© 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience, 1–6
tDCS improves dual task capacity 3
Data analysis
Primary study outcomes included measures related to gait and postural control, as well as the cost of performing a cognitive task on
gait and postural control. Secondary outcomes included cognitive
task performance within dual task trials. Within each assessment
period (i.e. before and after real and sham tDCS), outcome values
were averaged across the two trials completed within each experimental condition (i.e. gait: normal and dual task; postural control:
eyes open, eyes closed, dual task).
Gait outcomes included average gait speed and step duration variability. Gait speed (m/s) was calculated by dividing the distance
walked by the time taken to complete the trial. Stride duration variability (%) was determined by calculating the coefficient of variation
about the average step duration (i.e. the time between consecutive
heel-strikes) and multiplying by 100.
Postural control outcomes included average COP speed and area.
COP time series were first filtered using a 10 Hz low-pass filter to
minimise the potential effects of high-frequency measurement noise.
The COP speed (cm/s) was computed by dividing the total path
length by trial duration. The COP area (cm2) was determined by calculating the area of a confidence ellipse enclosing 95% of the COP
trajectory (Norris et al., 2005).
The cost of performing the cognitive task on each gait and postural control outcome (i.e. dual task cost) was determined by calculating the percent change in each variable from normal to dual task
conditions (Beauchet et al., 2008; Hausdorff et al., 2008; Ullmann
& Williams, 2010).
For each dual task trial, cognitive task performance was determined by calculating the error rate, i.e. the total number of mistakes
divided by the total number of responses.
between tDCS condition (real, sham) and time (pre-tDCS, posttDCS) was observed, such that gait speed appeared to be faster
following real tDCS as compared with sham tDCS and both
pre-tDCS assessments (Fig. 2). A significant interaction (F1,38 = 9.2,
P = 0.006) between tDCS condition and time was observed for the
dual task cost on gait speed (Fig. 4A). Post-hoc analyses revealed
that, within the real tDCS condition, performing the cognitive task
reduced gait speed less in the post-tDCS state as compared with
pre-tDCS, whereas sham tDCS had no effect on this outcome. tDCS
did not have a significant effect on step duration variability in either
walking condition, or the dual task cost on this variable.
The acute effects of tDCS on postural control are presented in
Figs 3 and 4. Neither real nor sham tDCS affected COP speed or
area when subjects stood quietly with eyes open or closed. Within
the dual task condition, however, significant interactions were
Fig. 2. The effects of noninvasive tDCS on gait speed in healthy young
adults. Gait speed was assessed immediately before and after both real and
sham tDCS targeting the left dlPFC. tDCS did not significantly alter gait
speed in the normal walking condition. In the dual task condition, subjects
appeared to walk faster following real tDCS only, but this trend did not
reach significance (P = 0.08). Error bars represent 1 SD from the mean.
Statistical analysis
Descriptive statistics were used to summarise the group characteristics and all primary and secondary study outcomes. The effect of
tDCS on each outcome was analysed using 2 9 2 repeatedmeasures ANOVAs. Model effects included tDCS condition (real,
sham), time (pre-tDCS, post-tDCS) and their interaction. Study outcomes obtained from each condition were analysed with a separate
model. The significance level was set to P = 0.05 for all analyses.
Tukey’s post-hoc testing was completed on significant models in
order to identify differences between variable means within each
tDCS condition and time point combination.
Results
Subject characteristics
All 20 subjects completed all study procedures. Seven subjects
received tDCS at the maximum intensity of 1.5 mA. The average
intensity for the entire cohort was 1.1 0.3 mA. Stimulation was
well tolerated by all subjects and was not associated with any selfreported adverse events.
The effects of transcranial direct current stimulation on gait
and postural control
The acute effects of tDCS on gait speed are presented in Figs 2
and 4. Neither real nor sham tDCS affected preferred gait speed
under the normal walking condition. During the dual task condition,
a trend (F1,38 = 3.5, P = 0.08) towards a significant interaction
Fig. 3. The effects of noninvasive tDCS on postural control in healthy
young adults. Postural control was assessed immediately before and after
both real and sham tDCS targeting the left dlPFC. tDCS did not alter postural control when subjects stood with eyes open or closed. As compared
with sham stimulation, however, real tDCS resulted in a significant reduction
in COP area and speed when standing while performing a cognitive task (i.e.
Dual Task). *Significant interaction (P < 0.05) between tDCS condition
(real, sham) and time (pre-tDCS, post-tDCS). Error bars represent 1 SD from
the mean.
© 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience, 1–6
4 J. Zhou et al.
A
B
C
Fig. 4. The effects of noninvasive tDCS on the cost of performing a cognitive dual task on gait and postural control. As compared with sham tDCS, real tDCS
reduced the dual task cost (i.e. the percent change from normal to dual task conditions) on gait speed (A) and standing postural sway speed (B) and area (C).
*Significant interaction (P < 0.05) between tDCS condition (real, sham) and time (pre-tDCS, post-tDCS). Error bars represent 1 SD from the mean.
observed between tDCS condition and time for both COP speed
(F1,38 = 7.3, P = 0.01) and area (F1,38 = 5.9, P = 0.01) (Fig. 3).
Post-hoc analyses revealed that, within the real tDCS condition,
COP speed was slower and COP area was smaller in the post-tDCS
assessment as compared with the pre-tDCS assessment. In contrast,
neither outcome was affected by sham tDCS. Similar statistical
interactions between tDCS condition and time were also observed
for the dual task cost on both COP speed (F1,38 = 6.1, P = 0.01)
and COP area (F1,38 = 6.8, P = 0.008) (Fig. 4B and C). Whereas
sham tDCS did not alter the dual task cost on either outcome as
compared with pre-test, real tDCS significantly reduced the dual task
cost on both outcomes.
The acute effects of transcranial direct current stimulation on
cognitive performance in dual task trials
The serial-subtraction task performance during cognitive dual task
trials was extremely high. When walking, the average number of
given responses was 19.2 4.8 and the average number of erroneous responses was 0.6 0.3, leading to an error rate of
3.5 2.0%. When standing, the number of given responses was
29.1 6.8 (note that standing trials were longer than walking trials), the number of errors was 0.9 0.4, and the error rate was
3.0 2.4%. The response numbers, error numbers and error rates
when standing or walking were unaffected by real or sham tDCS
(P = 0.5–0.8).
Discussion
This proof-of-concept, double-blind, sham-controlled study in
healthy young adults indicates that, as compared with sham stimulation, a single session of real tDCS reduced the cost of dual tasking
on multiple outcomes related to gait and postural control. Although
additional research is needed, these results provide strong preliminary evidence that modulation of dlPFC excitability may be one strategy to enhance the ability to stand and walk while simultaneously
performing secondary cognitive tasks in healthy young adult populations.
The dlPFC is a primary brain region supporting executive function (Kane & Engle, 2002), attention (Knight et al., 1995) and the
ability to perform more than one cognitive task at the same time
(Szameitat et al., 2002). Several recent structural and functional neuroimaging reports (Harada et al., 2009; Goble et al., 2011; Huppert
et al., 2012) indicate that the dlPFC is also involved in the control
of standing and walking. Rosano et al. (2008) reported that older
adults with less gray matter within the bilateral dlPFC tend to walk
with shorter steps and longer time spent with both feet on the
ground. Holtzer et al. (2011) utilised functional near-infrared spectroscopy to demonstrate that undisturbed walking induces bilateral
prefrontal cortex activation in healthy younger and older adults.
Interestingly, walking while performing a cognitive task (i.e. reciting
alternating letters of the alphabet) further increased prefrontal cortex
activation,but this effect was mitigated within the older group. Our
results extend this notion by demonstrating that, even in healthy
young adults, the experimental manipulation of cortical excitability
within the left dlPFC acutely improves outcomes related to gait and
postural control under dual task conditions.
There are several potential neurological mechanisms that may
have led to the tDCS-induced improvement in the ability to adapt
gait and posture to a cognitive stressor. To date, multiple theories
have been developed to explain the costs associated with cognitive
dual tasking (Yogev-Seligmann et al., 1999). The capacity-sharing
theory suggests that cognitive resources are limited in capacity and,
as a result, performing two tasks that require shared cognitive
resources will diminish performance in at least one of the tasks
(Tombu & Jolicoeur, 2003). In the current study, performing the
serial-subtraction task disrupted gait and postural control, suggesting
that these tasks require shared cognitive resources. As such, real
tDCS may have reduced observed detrimental dual task costs by
increasing the availability of cognitive resources and/or improving
the allocation of available resources to one or both tasks (Leite
et al., 2011; Filmer et al., 2013). However, the bottleneck theory of
dual task control posits that, if two tasks are processed by the same
neural networks, a ‘bottleneck’ occurs such that the processing of
one task will be delayed until the network or processor is free from
the other task (Ruthruff et al., 2001). Within this framework, tDCSrelated improvements may have stemmed from increased processing
speed and shortened time delay between two tasks (Pashler, 1994;
Redfern et al., 2001). In the current study, all subjects performed
the serial-subtraction task well and no tDCS-related changes in performance were observed (perhaps due to a ceiling effect). As more
difficult cognitive tasks require more activation with the dlPFC (and
other brain regions) (Szameitat et al., 2002), future work should
examine standing and walking during concurrent performance of
several cognitive tasks that vary in difficulty. This method would
enable further insight into the effects of tDCS on the interplay
between cognitive and motor function during both single and dual
task conditions. By choosing cognitive tasks that require rapid
© 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience, 1–6
tDCS improves dual task capacity 5
reaction to a presented stimulus (e.g. the n-back task), the effects of
tDCS on both resource allocation and processing speed, together
with their importance for gait and postural control, may also be
explored.
We chose a tDCS montage to target the left dlPFC because considerable work indicates that a single session of tDCS administered
with these parameters enhances cognitive task performance, particularly within verbal tasks requiring attention and short-term memory
(Fregni et al., 2005; Hecht et al., 2010; Javadi & Walsh, 2011;
Javadi et al., 2011; Gladwin et al., 2012; Metuki et al., 2012; Filmer et al., 2013). In the current study, it is unclear if the observed
tDCS-related reduction in the cognitive task costs to gait and postural control arose from specific neuronal changes with the left
dlPFC or from overall changes in brain excitability. The effects of
active tDCS targeting one or more other brain regions are therefore
worthy of investigation. For example, as the facilitation of excitability within the right dlPFC has also been shown to improve cognitive
performance, particularly in visual-based memory tasks (Rossi et al.,
2001; Gagnon et al., 2010), the impact of stimulating particular
brain regions may be dependent upon the type of cognitive dual task
being performed. Furthermore, in the current study, we did not measure the extent to which tDCS modulated cortical activity within different brain regions. Future work utilising single and paired-pulse
transcranial magnetic stimulation techniques to link the tDCSinduced changes in cortical neurophysiology with behavioral
changes is thus needed to elucidate the mechanisms underlying the
tDCS-induced reduction of dual task costs. Finally, tDCS alters cortical excitability by sending electrical currents between relatively
large electrodes placed upon the skin. The effects of tDCS on cortical excitability are therefore relatively diffuse and variable between
subjects (Datta et al., 2012). It is thus possible that tDCS-related
behavioral changes stemmed from altered cortical excitability within
other networks within the brain. To that end, the application of neuronavigation techniques (Datta et al., 2012) may optimise the individual effects of tDCS on cortical function and, thus, its beneficial
effect on standing and walking.
In conclusion, this study provides novel evidence in healthy
young adults that the modulation of cortical excitability improves
the ability to stand and walk while performing a secondary cognitive
task. Additional work is warranted to determine the extent to which
observed laboratory-based performance improvements transfer to
other environments (i.e. competitive sports). Moreover, as mounting
evidence suggests that daily tDCS treatments may result in persistent
changes in both cognitive function (Dockery et al., 2009) and sensorimotor performance (Zimerman et al., 2012), repeated tDCS
exposure may ultimately lead to long-term functional improvements.
Finally, as biological aging and numerous age-related diseases
appear to increase the role of cognition and underlying brain networks in the control of standing and walking (Manor et al., 2010;
Montero-Odasso et al., 2012b; Manor & Lipsitz, 2013), tDCS holds
great potential as a therapeutic balance intervention and fall-prevention strategy for these more vulnerable populations.
Acknowledgements
We would like to thank Dr Dapeng Bao and Dr Yang Hu from the Sport
Science Research Center at the Beijing Sport University for providing the
experimental balance equipment utilised in this study. A.P.-L. serves on the
scientific advisory boards for Nexstim, Neuronix, Starlab Neuroscience,
Neuroelectrics, and Neosync, and is listed as an inventor on several issued
and pending patents on the real-time integration of transcranial magnetic stimulation with electroencephalography and magnetic resonance imaging. This
study was supported by grants from the National Natural Science Foundation
of China (grant no. 11372013), the Sidnay Baer Foundation, and a KL2
Medical Research Investigator Training (MeRIT) award (1KL2RR025757-04)
from Harvard Catalyst/The Harvard Clinical and Translational Science Center
(UL 1RR025758). Study funders had no role in the study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Abbreviations
COP, center-of-pressure; dlPFC, dorsolateral prefrontal cortex; tDCS, transcranial direct current stimulation.
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